Overview of African Swine Fever

African swine fever (ASF) is a highly contagious hemorrhagic disease of pigs that produces a wide range of clinical signs and lesions that closely resemble those of classical swine fever (see Classical Swine Fever). It is an economically important disease that is enzootic in many African countries and the Mediterranean island, Sardinia. In June 2007, ASF was confirmed for the first time in Georgia in the Caucasus region. Since its introduction into Georgia, African swine fever virus (ASFV) has spread rapidly into vast areas of western and southern Russia, where it is currently (2013) circulating out of control in domestic and wild pig populations. The virus has spread to the edges of Europe, with outbreaks reported in both the Ukraine and Belarus in 2013, putting at risk the very large pig populations present in Eastern Europe.

Etiology and Epidemiology

ASFV is a large, enveloped, double-stranded DNA virus that replicates primarily in cells of the mononuclear phagocytic system. It is currently classified as the only member of a family called African swine fever–like viruses (Asfarviridae). The prolonged period during which ASF has been an enzootic disease in Africa is likely to have led to the selection of viruses of varying virulence. Distinct genotypes of ASFV have been differentiated by sequence analysis of the genomes of viruses obtained from different geographic areas over a long time. The virus is highly resistant to a wide pH range and to a freeze/thaw cycle and can remain infectious for many months at room temperature or when stored at 4°C. Virus in body fluids and serum is inactivated in 30 min at 60°C, but virus in unprocessed pig meat, in which it can remain viable for several weeks, can be inactivated only by heating to 70°C for 30 min. Although ASFV can be adapted to grow in cells from different species, it does not replicate readily in any species other than swine.

The disease is limited to all breeds and types of domestic pigs and European wild boar. All age groups are equally susceptible. In Africa, the virus produces inapparent infection in two species of wild swine—warthog (Phacochoerus aethiopicus) and bushpig (Potamochoerus porcus)—and in the soft tick Ornithodoros moubata. When the disease was endemic in southern Spain and Portugal, a different species of soft tick, O erraticus, became infected with the virus. Several other Ornithodoros spp that are not usually associated with pigs or wild swine have been infected experimentally. ASF has been reported in a large number of countries in Africa south of the Sahara, either as an enzootic disease or as sporadic epidemics in domestic pigs. The first spread of the disease outside Africa was into Europe (Portugal) in 1957 as a result of waste from airline flights being fed to pigs near Lisbon airport. Although this incursion of disease was almost certainly eradicated, a further outbreak occurred in 1960 in Lisbon, and ASF then remained endemic in the Iberian peninsula until the mid-1990s. Outbreaks of ASF were reported in a number of other European countries during the 20th century, including Malta (1978), Italy (1967, 1980), France (1964, 1967, 1977), Belgium (1985), and the Netherlands (1986). The disease was eradicated from each of these countries but has remained endemic in Sardinia since its introduction in 1978. During the 1970s, ASFV spread to the Caribbean and South America. An outbreak in south Brazil in 1978–1979 was eradicated by stamping out, and Brazil regained its ASF-free status in December 1984.

The spread of ASF out of Africa has been a relatively rare event, but in June 2007 ASF was confirmed in pigs in the former Soviet republic of Georgia in the Caucasus region. Genetic analysis revealed the genotype of the Georgia isolate to be closely related to isolates in circulation in Mozambique, Madagascar, and Zambia. It is therefore likely that pigs were fed ASFV-contaminated pig meat transported by ship from the southeastern part of Africa. By July 2007, the outbreak had spread to 56 of 61 districts in Georgia; soon after, outbreaks of ASF were reported in neighboring regions, including the autonomous republic of Abkhazia, Armenia, and Nagorno-Karabakh. Later in the year, infection of wild boar was confirmed in the Russian republic of Chechnya. In 2008, the spread of ASF continued into North Ossetia; it then jumped over 1,000 km into Orenburg, illustrating its potential for rapid spread over long distances. By October 2008, a total of 21 outbreaks of ASF had been officially reported in five Russian administrative divisions. From 2009–2013, the virus has continued to spread within the Russian Federation, and there are currently (Oct 2013) two main expanding hotbeds of infection in Russia, one in the southern part of the center of the Rostov region (Oblast) and the other in the Tver region (Oblast) and the adjoining areas. In 2013, outbreaks of ASF were reported in both the Ukraine and Belarus, putting at risk large pig populations in eastern Europe.

Transmission and Pathogenesis

ASFV is maintained in Africa by a natural cycle of transmission between warthogs and the soft tick vector O moubata, which inhabits warthog burrows and from which it is unlikely ever to be eliminated. The spread of virus from the wildlife reservoirs to domestic pigs can be by the bite of an infected soft tick or by ingestion of warthog tissues. Virulent viruses produce acute disease, and all body fluids and tissues contain large amounts of infectious virus from the onset of clinical disease until death. Pigs infected with less virulent isolates can transmit virus to susceptible pigs as long as 1 mo after infection; blood is infectious for as long as 6 wk, and transmission can occur if blood is shed. Pigs usually become infected via the oronasal route by direct contact with infected pigs or by ingestion of waste food containing unprocessed pig meat or pig meat products. The primary route of infection is the upper respiratory tract, and virus replicates in the tonsil and lymph nodes draining the head and neck, with generalized infection rapidly following via the bloodstream. High concentrations of virus are then present in all tissues. The factors that produce the hemorrhagic lesions are not fully defined, but severe disruption to the blood clotting mechanism plays a major role. Virus is excreted mainly from the upper respiratory tract and is also present in secretions and excretions containing blood.

Pigs that survive infection with the less virulent isolates may be persistently infected and have circulating antibody, although they do not excrete virus or transmit virus to their offspring in utero. Their role in the epidemiology of the disease is not fully understood; however, they are resistant to disease when challenged with related highly virulent isolates, indicating some level of cross-protective immunity between strains.

Clinical Findings and Lesions

Peracute, acute, subacute, and chronic forms of ASF occur, and mortality rates vary from 0 to 100%, depending on the virulence of the virus with which pigs are infected. Acute disease is characterized by a short incubation period of 3–7 days, followed by high fever (up to 42°C) and death in 5–10 days. The least variable clinical signs are loss of appetite, depression, and recumbency; other signs include hyperemia of the skin of the ears, abdomen, and legs; respiratory distress; vomiting; bleeding from the nose or rectum; and sometimes diarrhea. Abortion is sometimes the first event seen in an outbreak. The severity and distribution of the lesions also vary according to virulence of the virus. Hemorrhages occur predominantly in lymph nodes, kidneys (almost invariably as petechiae), and heart; hemorrhages in other organs are variable in incidence and distribution. Some isolates produce an enlarged and friable spleen; straw-colored or blood-stained fluid in pleural, pericardial, and peritoneal cavities; or edema and congestion of the lungs. Some viruses of low virulence have been isolated in Europe and produce nonspecific clinical signs and lesions. Chronic disease is characterized by emaciation, swollen joints, and respiratory problems. This form of the disease is rarely seen in outbreaks.

Diagnosis

ASF cannot be differentiated from classical swine fever (hog cholera) by either clinical or postmortem examination. Samples of blood, serum, spleen, tonsil, and gastrohepatic lymph nodes from suspected cases should be submitted to the laboratory for confirmation. Virus can be isolated by inoculation of primary cultures of pig monocytes, in which it produces hemadsorption of pig red cells to the surface of infected cells. Classical swine fever virus does not replicate in these cells. There are nonhemadsorbing viral isolates, some of which produce virulent disease. These isolates produce only a cytopathic effect in pig leukocytes. Confirmation of ASF in these cases has to be performed by either PCR or an antigen-detection ELISA. Viral antigen can be detected in infected tissue smears or sections by staining with labeled antibodies (several enzyme-labeled tests are available, eg, immunofluorescence), and viral DNA by PCR or hybridization of nucleic acid probes to tissue sections. The most appropriate tests to detect antibody in serum or tissue fluids are the ELISA and indirect immunofluorescence.

Other differential diagnoses include hemorrhagic bacterial infections and certain types of poisons.

Control

There is no treatment for ASF, and all attempts to develop a vaccine have so far been unsuccessful. Prevention depends on ensuring that neither infected live pigs nor pig meat products are introduced into areas free of ASF. All successful eradication programs have involved the rapid diagnosis, slaughter, and disposal of all animals on infected premises. Sanitary measures must also be applied and include control of movement and treatment of waste food. Subsequently, a serologic survey of all pig farms within a specific control zone must be conducted to ensure that all infected pigs have been identified.

Last full review/revision November 2013 by Chris Oura, BVetMed, MSc, PhD, MRCVS